Skip to content


  • Letter to the Editor
  • Open Access

Individual differences in autistic traits predict the perception of direct gaze for males, but not for females

  • 1Email author,
  • 2,
  • 3,
  • 3,
  • 2 and
  • 1
Molecular Autism20145:12

  • Received: 24 October 2013
  • Accepted: 16 January 2014
  • Published:


Despite the emphasis of autism spectrum disorders as a continuum of atypical social behaviors and the sexual heterogeneity of phenotypic manifestations, whether gaze processing constitutes an autistic endophenotype in both sexes remains unclear. Using the Autism-Spectrum Quotient and a psychophysical approach in a normal population (N = 128), here we demonstrated that individual differences in autistic traits predicted direct-gaze perception for males, but not for females. Our findings suggest that direct-gaze perception may not constitute an autistic endophenotype in both sexes, and highlight the importance of sex differences when considering relationships between autistic traits and behaviors.


  • Direct gaze
  • Individual differences
  • Sex differences
  • Autistic traits
  • Autism spectrum disorders (ASD)


Individuals with autism spectrum disorders (ASD) exhibit atypical behavior in perceiving others’ eye gaze and eye contact, a crucial factor underlying social communication [1, 2]. Their heterogeneity of phenotypic manifestations has led researchers to suggest that autistic traits are extending into the normal population [3, 4]. Besides individual heterogeneity, sexual heterogeneity of phenotypes has also been suggested in individuals with ASD [5]. However, whether gaze processing constitutes an autistic endophenotype in both sexes remains unclear. By examining the relationship between performance in perceiving direct gaze and the scores on the Autism-Spectrum Quotient (AQ) [6] in a normal population, we show that individual differences in autistic traits predict performance in direct-gaze perception for males, but not for females.

Each trial started with the 20-ms presentation of a face or geometric control stimulus (Figure 1a). Face images were looking either directly toward the participant (0°), or left- or right-averted by 10°, 20°, or 30° (see Additional file 1). The control geometric stimuli (a black box embedded in a white rectangle) were adjusted to match the mean apparent sclera-iris ratio of the face images. All stimuli were followed by a 100-ms mask. A variable inter-stimulus interval (ISI) was used to control task difficulty (20, 40, or 60 ms). Following the mask, a fixation cross was presented until a response was obtained.
Figure 1
Figure 1

Experimental paradigm and results. (a) Schematic presentation of the experimental task. The two tasks were performed in four separate blocks, each containing 144 trials, with the order counterbalanced across participants. (b) Correlation between the Autistic-Spectrum Quotient (AQ) score and direct-gaze threshold (estimated angle of 50% ‘direct’ response). A significant correlation was observed in male, but not female participants. A significant correlation between the AQ score and geometric (control) threshold was not observed in both sexes.

Participants (64 females, 64 males) were required to indicate whether the eyes were looking directly at them for the gaze task. They were required to indicate whether the black box was in the center of the white rectangle for the geometric control task. Gaze/geometric threshold is defined as the angle at which a 50% direct/center response is achieved, as estimated by fitting a logistic function to each observer’s responses [7] (Additional file 1: Figure S1). A lower threshold indicates higher sensitivity in direct/center perception. Participants also completed the AQ, a questionnaire that assesses autistic traits in normal adults [6].

A significant correlation was observed between the AQ score and gaze threshold in male (r = -.378, P = .002), but not female participants (r = .012, P = .925) (Figure 1b). Significant correlations were not found between the AQ score and geometric threshold in male (r = -.227, P = .071) or female participants (r = -.084, P = .508) (Additional file 1: Figure S2). A correlation between the AQ score and gaze threshold was greater in male than in female participants (z = 2.260, P = .024). The correlation between the AQ score and geometric threshold was similar between male and female participants (z = .809, P = .407). In addition, a partial correlation (controlling for the geometric threshold) between the AQ score and gaze threshold was significant in male (r = -.312, P = .013), but not in female participants (r = .028, P = .828), which indicated that the significant correlation was not attributed to low-level discrimination acuity, but was specific to gaze processing. The higher sensitivity in males with high AQ scores may reflect a shift toward typically-developing females [8] and/or higher dependency on low-level visual information in gaze processing [9] (see Additional file 1).

Our results clearly demonstrated that the relationship between gaze perception and autistic traits measured by the AQ may differ between male and female individuals. The perception of direct gaze may constitute an autistic endophenotype in the normal population for males, but not for females. As mechanisms underlying sex differences in the prevalence and phenotypic manifestation of ASD appear to be multifactorial [5, 10], at least two possible explanations exist for our findings; these are as follow.

First, female protective factors may underlie sex differences in our study. Recent studies have demonstrated the necessity of a greater genetic load to present autistic behaviors in females than in males [11, 12] and have also suggested that some genetic factors related to the female sex protect them against autistic behavior [5, 13]. Furthermore, females may learn to effectively mask or camouflage their autistic behaviors through their development and/or experience as female [14]. It is likely that these genetic and non-genetic female protective factors modulate the processing of direct gaze in the general population, rendering the autistic-trait dependency of behavior, which is found in males, invisible in females.

Second, the autistic traits measured by the AQ may not necessarily reflect all autistic behaviors in both sexes and/or may be somewhat male-biased. Consequently, although the AQ does not include an item directly asking about eye gaze, the autistic traits measured by the AQ may be linked with the perception of direct gaze in males only, and not in females. If this is partly valid, our results may imply that gaze processing in females is mediated by, if not totally, distinct mechanisms from males [15].

In conclusion, our results demonstrated the sex-differential correlational-patterns between autistic traits and direct-gaze perception in the general population that may further extend into the extremes of autistic trait distribution (that is, individuals with a clinical diagnosis of autism). More generally, our findings highlight the importance of sex differences when considering relationships between autistic traits and a range of cognitive/behavioral functions, including gaze perception and gaze behavior. Future studies are needed to examine sex differences in order to capture autistic endophenotypes accurately.



autism spectrum disorders


Autism-Spectrum Quotient


inter-stimulus interval.



This study was supported by grants from the Japan Society for the Promotion of Science #23700315 to DM, #22220003 to HA, #24300279 to KW; and CREST, Japan Science and Technology Agency to KW. The use of the face image in Figure 1 is acknowledged by the photographed model with a written informed consent.

Authors’ Affiliations

Research Center for Advanced Science and Technology, The University of Tokyo, 4-6-1 Komaba, Meguro Tokyo, 153-8904, Japan
Department of Psychology, Graduate School of Letters, Kyoto University, Yoshida-honmachi, Sakyo, Kyoto 606-8501, Japan
College of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro Tokyo, 153-8902, Japan


  1. Emery NJ: The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev. 2000, 24: 581-604. 10.1016/S0149-7634(00)00025-7.View ArticlePubMedGoogle Scholar
  2. Senju A, Johnson MH: Atypical eye contact in autism: models, mechanisms and development. Neurosci Biobehav Rev. 2009, 33: 1204-1214. 10.1016/j.neubiorev.2009.06.001.View ArticlePubMedGoogle Scholar
  3. Spiker D, Lotspeich LJ, Dimiceli S, Myers RM, Risch N: Behavioral phenotypic variation in autism multiplex families: evidence for a continuous severity gradient. Am J Med Genet. 2002, 114: 129-136. 10.1002/ajmg.10188.View ArticlePubMedGoogle Scholar
  4. Constantino JN, Todd RD: Autistic traits in the general population: a twin study. Arch Gen Psychiatry. 2003, 60: 524-530. 10.1001/archpsyc.60.5.524.View ArticlePubMedGoogle Scholar
  5. Werling DM, Geschwind DH: Sex differences in autism spectrum disorders. Curr Opin Neurol. 2013, 26: 146-153. 10.1097/WCO.0b013e32835ee548.PubMed CentralView ArticlePubMedGoogle Scholar
  6. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E: The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord. 2001, 31: 5-17. 10.1023/A:1005653411471.View ArticlePubMedGoogle Scholar
  7. Wichmann FA, Hill NJ: The psychometric function: I. Fitting, sampling, and goodness of fit. Percept Psychophys. 2001, 63: 1293-1313. 10.3758/BF03194544.View ArticlePubMedGoogle Scholar
  8. Lai M-C, Lombardo MV, Suckling J, Ruigrok ANV, Chakrabarti B, Ecker C, Deoni SCL, Craig MC, Murphy DGM, Bullmore ET: Biological sex affects the neurobiology of autism. Brain. 2013, 136: 2799-2815. 10.1093/brain/awt216.PubMed CentralView ArticlePubMedGoogle Scholar
  9. Senju A, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H: Is anyone looking at me? Direct gaze detection in children with and without autism. Brain Cogn. 2008, 67: 127-139. 10.1016/j.bandc.2007.12.001.View ArticlePubMedGoogle Scholar
  10. Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R: Why are autism spectrum conditions more prevalent in males?. PLoS Biol. 2011, 9: e1001081-10.1371/journal.pbio.1001081.PubMed CentralView ArticlePubMedGoogle Scholar
  11. Levy D, Ronemus M, Yamrom B, Y-h L, Leotta A, Kendall J, Marks S, Lakshmi B, Pai D, Ye K: Rare de novo and transmitted copy-number variation in autistic spectrum disorders. Neuron. 2011, 70: 886-897. 10.1016/j.neuron.2011.05.015.View ArticlePubMedGoogle Scholar
  12. Gilman SR, Iossifov I, Levy D, Ronemus M, Wigler M, Vitkup D: Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron. 2011, 70: 898-907. 10.1016/j.neuron.2011.05.021.PubMed CentralView ArticlePubMedGoogle Scholar
  13. Robinson EB, Lichtenstein P, Anckarsäter H, Happé F, Ronald A: Examining and interpreting the female protective effect against autistic behavior. Proc Natl Acad Sci U S A. 2013, 110: 5258-5262. 10.1073/pnas.1211070110.PubMed CentralView ArticlePubMedGoogle Scholar
  14. Lai M-C, Lombardo MV, Pasco G, Ruigrok ANV, Wheelwright SJ, Sadek SA, Chakrabarti B, Baron-Cohen S, Consortium MA: A behavioral comparison of male and female adults with high functioning autism spectrum conditions. PLoS One. 2011, 6: e20835-10.1371/journal.pone.0020835.PubMed CentralView ArticlePubMedGoogle Scholar
  15. Moriuchi JM, Klin A, Jones W: Sex differences in dynamic visual scanning patterns in school-age children with autism spectrum disorders. International Meeting for Autism Research. 2013, Donostia/San Sebastián, SpainGoogle Scholar


© Matsuyoshi et al.; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated.